Keywords acute kidney injury, acute renal failure, RIFLE criteria Curr Opin Crit Care 12:531–537.. Kellum, MD, Department of Critical Care Medicine, University of Pittsburgh, Room 608, S
Trang 1Eric A.J Hostea,b and John A Kellumb
Purpose of review
To review recent advances in the definitions and diagnostic
criteria for acute renal failure and acute kidney injury To
explore how these changes impact the epidemiology and
clinical implications for patients in the intensive care unit
Recent findings
Recently published consensus criteria for the definition of
acute renal failure/acute kidney injury have led to significant
changes in how we think about this disorder Studies from
around the world, both in and out of the intensive care unit,
have shown a dramatic incidence of acute kidney injury and
high associated mortality This review considers these new
findings and their historical context, and attempts to shed
new light on this old problem
Summary
Small changes in kidney function in hospitalized patients are
important and impact on outcome RIFLE criteria provide a
uniform definition of acute kidney injury and are increasingly
used in literature
Keywords
acute kidney injury, acute renal failure, RIFLE criteria
Curr Opin Crit Care 12:531–537 ß 2006 Lippincott Williams & Wilkins.
a
Intensive Care Unit, Ghent University Hospital, Ghent, Belgium and b
The Clinical Research, Investigation and Systems Modeling of Acute Illness (CRISMA)
Laboratory, Department of Critical Care Medicine, University of Pittsburgh, School
of Medicine, Pittsburgh, Pennsylvania, USA
Correspondence to John A Kellum, MD, Department of Critical Care Medicine,
University of Pittsburgh, Room 608, Scaife Hall, 3550 Terrace Street, Pittsburgh,
PA 15261, USA
Tel: +1 412 647 6966; fax: +1 412 647 8060; e-mail: kellumja@ccm.upmc.edu
Current Opinion in Critical Care 2006, 12:531–537
Abbreviations
AKI acute kidney injury
ARF acute renal failure
GFR glomerular filtration rate
ICU intensive care unit
MDRD modification of diet in renal disease
RRT renal replacement therapy
ß 2006 Lippincott Williams & Wilkins
1070-5295
Introduction
For most clinicians working in intensive care and nephrology, the notion of acute renal failure (ARF) is that of severe organ dysfunction For research and even reimbursement purposes, ARF is often defined by the need for artificial support, termed renal replacement therapy (RRT) This narrow concept of ARF may, how-ever, be far too limiting, and mounting evidence suggests that acute dysfunction of kidney manifest by changes in urine output and blood chemistries portend serious clinical consequences [1]
The term ARF is relatively new in the medical lexicon Eknoyan [2] reminds us that the first description of ARF, then termed ischuria renalis, was by William Heberden
in 1802 At the beginning of the 20th century, ARF, then named acute Bright’s disease, was well described in William Osler’s early works (1909), as a consequence of toxic agents, pregnancy, burns, trauma or operations on the kidneys During World War I the syndrome was named ‘War Nephritis’ [3] and was reported in several publications The syndrome was forgotten until World War II, when Bywaters and Beall [4] published their classical paper on crush syndrome It was Homer W Smith [5] who is credited with the introduction of the term ‘ARF’, in a chapter on ‘Acute renal failure related to traumatic injuries’, in his textbook The Kidney – Structure and Function in Health and Disease (1951) The same year a whole issue of the Journal of Clinical Investigation was dedicated to ARF [6]
In most reviews and textbooks [7,8], the concept of acute kidney dysfunction still emphasizes the most severe forms with severe azotemia and often with oliguria or anuria It is only in the past few years that moderate decreases of kidney function have been recognized as important, e.g by the Sepsis-related Organ Failure Assessment score [9] and in studies on radiocontrast-induced nephropathy [10]
Moreover, until very recently there was no consensus on the diagnostic criteria or clinical definition of ARF, resulting in multiple different definitions A recent sur-vey revealed the use of at least 35 definitions in the literature [11] Apart from differences in patient charac-teristics, this is probably one of the main reasons that there is such a wide variation in the reported incidence and outcome of ARF (incidence ranges between 1 and 31% [12,13] and mortality between 28 and 82% [13,14]) Obviously, if one study defines ARF as a 25% or greater
Trang 2rise in serum creatinine and another study defines ARF
only as the need for RRT, the two studies will not
describe the same cohort of patients There is even a
linear correlation between the degree of kidney
dysfunc-tion and the outcome of acute kidney dysfuncdysfunc-tion The
more strict the definition of ARF, the greater the
mortality (Fig 1) [11]
Another element that has emerged in recent years is the
observation that small decreases in kidney function are
important For example, Levy et al [10] found that a 25%
increase of serum creatinine after administration of
radio-contrast was associated with a worse outcome compared
with those who did not experience a 25% or greater
increase Chertow et al [15] defined hospital acquired
acute kidney dysfunction as an increase of serum
crea-tinine of above 0.3 mg/dl and found that this was
inde-pendently associated with mortality
Similarly, Lassnig et al [16] saw, in a cohort of patients
who underwent cardiac surgery, that acute kidney
dys-function, defined as an increase of serum creatinine of
0.5 mg/dl or above or a decrease greater than 0.3 mg/dl,
was associated with worse survival The reasons why
small alterations in renal function lead to increases in
hospital mortality are unclear Possible explanations
include the untoward effects of acute kidney dysfunction
such as volume overload, retention of uremic compounds,
acidosis, electrolyte disorders, increased risk for infection
and anemia [17] Although acute kidney dysfunction
could simply be co-linear with unmeasured variables that
lead to increased mortality, multiple attempts to control
for known clinical variables has led to the consistent
conclusion that renal dysfunction is independently
associated with outcome Furthermore, more severe renal dysfunction tends to be associated with even worse out-come compared with milder abnormalities
Acute kidney injury and the RIFLE criteria
Recognizing that early and/or milder forms of renal dysfunction have clinical importance and that staging (mild to severe) is desirable in order to better describe the syndrome, the Acute Dialysis Quality Initiative, a group of experts in acute kidney dysfunction, con-sisting of nephrologists and intensivists, proposed the RIFLE criteria for acute kidney dysfunction (http:// www.ccm.upmc.edu/adqi/ADQI2/ADQI2g1.pdf) [18] The acronym RIFLE stands for the increasing severity classes Risk, Injury and Failure, and the two outcome classes Loss and End-Stage Kidney Disease The three severity grades are defined on the basis of the changes in serum creatinine or urine output (Fig 2) where the worst
of each criterion is used The two outcome criteria, Loss and End-Stage Kidney Disease, are defined by the duration of loss of kidney function
The RIFLE criteria were published as a workgroup document on the Acute Dialysis Quality Initiative web-site in June 2003, published online in May 2004 and in print in August 2004 [18] Since then a number of papers have been published that use the RIFLE criteria [19,20,21,22,23,24,25,26,27,28,29] (Table 1) Most of the studies were published in the past year
Figure 1 Relationship between the definition used of acute
renal failure (ARF) and the corresponding mortality observed
Seventeen published definitions of ARF were classified into grades on
the basis of the criteria used As an arbitrary reference, a definition
requiring a doubling of serum creatinine or a rise in serum creatinine by
1 mg/dl was given a grade of 2 More strict criteria were given
propor-tionally high grades and less strict criteria, lower grades The
corre-sponding observed mortality in the control group (for clinical trials) or
overall mortality (for observational studies) were then charted There was
a significant correlation between the definition grade and observed
mortality From Kellum et al [11]; used with permission.
Figure 2 The RIFLE classification scheme for acute kidney injury
Risk
Injury
Failure
Loss ESRD
Increased creatinine ×1.5 or GFR decrease > 25%
End-stage renal disease
Urine output criteria GFR criteria
UO < 0.3 ml/kg/h
× 24 h or Anuria × 12 h
UO < 0.5 ml/kg/h
× 12 h
UO < 0.5 ml/kg/h
× 6 h
Increased creatinine × 2
or GFR decrease > 50%
Increase creatinine ×3
or GFR decrease >75%
or creatinine ≥ 4 mg/dl
(Acute rise of ≥ 0.5 mg/dl)
High sensitivity
High specificity
Persistent ARF = complete loss of renal function > 4 weeks
Oliguria
The classification system includes separate criteria for serum creatinine and urine output (UO) The criteria that lead to the worst possible classification should be used Note that RIFLE-F is present even if the increase in serum creatinine is below 3-fold so long as the new serum creatinine is 4.0 mg/dl (350 mmol/l) or above in the setting of an acute increase of at least 0.5 mg/dl (44 mmol/l) The shape of the figure denotes the fact that more patients (high sensitivity) will be included in the mild category, including some without actually having renal failure (less specificity) In contrast, at the bottom, the criteria are strict and therefore specific, but some patients will be missed GFR, glomerular filtration rate; ARF, acute renal failure From Bellomo et al [18]; used with permission.
Trang 3In addition, the Acute Kidney Injury Network
organized two conferences endorsed by the different
critical care and nephrology societies The aim of these
conferences was to come to a broader consensus on
the definitions and terminology for ARF In particular,
this group has proposed the term ‘AKI’ to define the entire spectrum of acute renal dysfunction from its earliest and mildest forms to the need for RRT We will therefore adopt this term, as we have previously [1,25]
Table 1 Papers in which the RIFLE criteria for AKI were used
Cohort Aim of the study
AKI defined
on glomerular filtration rate (1)
or urine output and glomerular filtration rate (2)
Outcome criteria
Occurrence
of AKI RIFLE max
Herget-Rosenthal
et al [19]
85 ICU patients, with initial normal GFR
evaluation of cystatin
C vs creatinine
1 no 44/85 (51.8%) R: 3/85 (3.5%)
I: 13/85 (15.3%) F: 28/85 (32.9%) Hoste et al [20] 704 AKI patients
treated with RRT
impact of BSI NA yes NA L: no BSI 9.2%/
BSI 43.5%
E: no BSI 0.5%/ BSI 8.1%
Bell et al [21]a 207 continuous
RRT patients
long-term outcome 2 yes NA R: 17/207 (8.2%)
I: 50/207 (24.2%) F: 121/207 (58.5%) L: 3/207 (1.4%) E: 16/207 (7.7%) Abosaif
et al [22]a
183 ICU patients with AKI on admission
outcome 2 no NA R: 60/159 (37.7%)
I: 56/159 (35.2%) F: 43/159 (27.0%) Kuitunen
et al [23]
813 cardiac surgery patients
incidence and outcome of AKI
2 no 156/813 (19.2%) R: 88/813 (10.8%)
I: 28/813 (3.4%) F: 40/813 (4.9%) Guitard
et al [24]
94 liver transplant patients
incidence and outcome of AKI
1 no 60/94 (63.8%) I: 39/94 (41.5%)
F: 21/94 (22.3%) Hoste
et al [25]
5383 ICU patients
incidence and outcome of AKI
2 no 3617/5383 (67.2%) R: 670/5383 (12.4%)
I: 1436/5383 (26.5%) F: 1511/5383 (28.1%) Uchino
et al [26]
20 126 patients admitted to the hospital
incidence and outcome of AKI
I: 5.2%
F: 3.7%
Lin et al [27] 46 ECMO
patients
incidence and outcome of AKI
2 no 36/46 (78.3%) R: 7/46 (15.2%)
I: 18/46 (39.1%) F: 11/46 (23.9%) Heringlake
et al [28]
29 623 cardiac surgery patients
incidence and outcome of AKI
1 no 15.4% (range 3.1–75%) R: 9% (2–40%)
I: 5% (0.8–30%) F: 2% (0.6–33%) Lopes et al [29] b 126 burn
patients
incidence and outcome of AKI
2 no 35.7% R: 14.3%
I: 8.7%
F: 12.7%
R, RIFLE Risk class; I, RIFLE Injury class; F, RIFLE Failure class; L, RIFLE Loss; E, RIFLE End-Stage Kidney Disease AKI, acute kidney injury; BSI, bloodstream infection; ICU, intensive care unit; NA, not available/applicable; RRT, renal replacement therapy.
a
Patients were classified at inclusion in the study (on admission to the ICU or at start of continuous RRT).
b Patients were classified on occurrence of maximum RIFLE class during the first 10 days of hospital admission.
Trang 4Use of the RIFLE criteria
An overview of the papers that used the RIFLE criteria
for AKI is presented in Table 1 All studies used the
severity grading criteria Risk, Injury and Failure, but only
two studies [20,21] also used the outcome criteria Loss
and End-Stage Kidney Disease Both studies that used
the outcome criteria were in a cohort of AKI patients
defined by the need for RRT Only Bell et al [21]
classified both severity grades and outcome classes All
patients included in this study were treated with
con-tinuous RRT for AKI They had therefore severe AKI
and there is rationale to classify these as Failure,
accord-ing to the adaptations made to the RIFLE criteria after
the First Acute Kidney Injury Network Conference
(personal communication)
Severity grading was performed according to the RIFLE
criteria on creatinine and urine output criteria in seven
out of the 10 studies that reported on severity grading
[21,22,23,24,25,27,29] Lin et al [27], however,
used different urine output criteria cut-offs compared
with those of RIFLE The three remaining studies
defined severity of AKI on a change of serum creatinine
level and not on urine output [19,26,28] The reasons
for this were diverse Herget-Rosenthal et al [19]
com-pared assessment of glomerular filtration rate (GFR) by
serum creatinine and cystatin C levels Uchino et al [26]
retrospectively evaluated hospital-wide cases, which
pre-vented assessment of urine output In addition, the study
by Heringlake et al [28] was a large prospective study on
practice patterns in cardiac surgery in German
cardiovas-cular centers Presumably, the study coordinators chose
to keep the questionnaire as compact as possible in order
to get a large enough response
Interestingly, one group chose to use the Cockcroft–Gault
equation for assessment of GFR, rather than use a change
in serum creatinine levels as all other authors did [22]
When baseline serum creatinine level is unknown in a
patient without a history of chronic kidney insufficiency,
the Acute Dialysis Quality Initiative proposed the use of
a baseline creatinine based upon the modification of diet
in renal disease (MDRD) equation assuming a
GFR > 75 ml/min/1.73 m2 [18] This was done in only
three studies [25,26,27] Kuitunen et al [23] also
used the MDRD formula, although not for assessment of
a baseline creatinine level, but for assessment of GFR
Most studies used the RIFLE criteria to assess the
occurrence rate of AKI in specific cohorts of patients
Two studies, however, used the RIFLE criteria for other
means than this Herget-Rosenthal et al [19] evaluated
whether a serum level of cystatin C is a better marker for
GFR than a serum creatinine level and Hoste et al [20]
used the RIFLE outcome criteria as a secondary outcome
parameter in a study on the impact of bloodstream infection in AKI patients treated with RRT
Occurrence rate of acute kidney injury defined
by the RIFLE criteria
The occurrence rate of AKI defined by RIFLE criteria in the different cohorts ranged from 15.4 to 78.3% (Table 1) This is higher than generally accepted when the classic terminology of ARF is used The large study by Uchino
et al [26] demonstrated that almost 18% of hospitalized patients in a large tertiary care hospital had an episode of AKI defined by RIFLE on GFR criteria This is much higher than the incidence of 7.2% reported in a hallmark study on data from 1996 [30] and 4.9% in the same hospital
on data from 1979 [31] Although the definition of AKI used in that study differs from the RIFLE criteria, the sen-sitivity seems comparable Nash et al and Hou et al [30,31] defined AKI as a rise in serum creatinine above 0.5 mg/dl for patients with a baseline below 1.9 mg/dl, above 1.0 mg/dl for patients with a baseline of 2–4.9 mg/dl and above 1.5 mg/dl for patients with serum creatinine level above 5.0 mg/dl An explanation for this may be that RIFLE criteria are more sensitive, especially for patients with acute or chronic disease; alternatively, the three cohorts may also have different baseline characteristics and/or different comorbidities The trend of increasing incidence for the same definition in the same institute suggests that the latter explanation seems more plausible Increasingly, patients are now older, suffer from more comorbidity such as diabetes or cardiovascular disease, and more patients are exposed to diagnostic and thera-peutic procedures with potential harm for kidney function The two large studies in cardiac surgery patients indicate that the incidence of AKI after cardiac surgery is about 15–20% [23,28] This is a considerably higher inci-dence compared to the inciinci-dence of ARF of below 8% as
is generally accepted in this specific cohort of patients [12,32 –35]
In a single-center, tertiary care, general intensive care unit (ICU) setting, two patients out of three experienced
an episode of AKI [25] Again, this is a considerably higher incidence of renal dysfunction than generally reported (generally around 5% [36] up to 31% in specific subgroups [13,37]) Finally, small studies [24,27,29] in specific groups of patients such as patients with cardio-genic shock on extracorporeal membrane oxygenation, liver transplantation or burns also demonstrated high ICU period prevalence rates for AKI of 78, 64 and 35.7%, respectively
In summary, the RIFLE criteria for AKI are certainly more sensitive compared with more traditional defi-nitions of ARF The incidence of AKI defined by the RIFLE criteria is much higher (2–10 times higher) than
Trang 5the incidence of ARF, but the incidence for both appears
to be increasing
Outcome of acute kidney injury defined by
RIFLE criteria
An overview of mortality for the individual grades of AKI
in various populations is presented in Fig 3 Importantly,
all studies, with the exception of Bell et al [21], report a
stepwise increase of mortality for increasing RIFLE class
The study by Bell et al is, however, an exception in this
series, as it included only patients that were treated with
continuous RRT, suggesting that these patients already
had severe AKI In all other studies, increasing severity
classes of AKI indeed had worse outcome
In four studies, a multivariable analysis was performed to
assess the impact of AKI defined by RIFLE after
correc-tion for other comorbidities (Table 2) AKI defined by
RIFLE criteria was associated with worse outcome in all
four studies
Limitations of RIFLE criteria
From the preceding discussion we can distill some of the
limitations of the RIFLE criteria Urine output criteria
were not used in four studies Although decreased urine
output has a high specificity and sensitivity for acute
kidney dysfunction, the urine output criteria also
come with limitations First, sensitivity and specificity
may be lost when diuretics are used The use of diuretics
is not explicitly addressed in the RIFLE criteria,
although their use is common practice worldwide in
AKI patients (reported incidences from 59 to 70%)
[38,39] The urine output criteria can only be accurately
assessed in patients with a urinary catheter Thus, the use
of urine output criteria may be limited to the ICU cohort
These data may, however, also prompt us to reconsider
and improve the rigor by which urine output is currently collected in most areas outside the ICU or operating room Another limitation of the urine output criteria is that there are many caveats that prevent exact measure-ment of urine output, e.g obstruction of the urine bladder catheter by debris or blood clots, kinking of the catheter, etc Finally, it may also be that the urine output criteria for Risk, Injury and Failure are not well balanced with the respective creatinine criteria, and are too sensitive In other words, Risk patients defined by creatinine criteria are more severely ill compared with Risk patients defined
Figure 3 Mortality in the different studies for individual RIFLE classes
0 10 20 30 40 50 60 70 80 90 100
Mortality (%)
Lopes Uchino Lin
Hoste Kuitunen Abosaif Bell
Risk Injury Failure
Table 2 Outcome of AKI defined by RIFLE criteria and by individual RIFLE severity grades after correction for other comorbidities
Statistical test used
RIFLE criteria
OR (for LR)/
HR (for CPH) (95% confidence interval) P Kuitunen
et al [23]
LR AKI OR: 2.616 <0.001 Hoste
et al [25]
CPH AKI HR: 1.7
(1.28–2.13)
<0.001 CPH risk HR: 1.0
(0.68–1.56)
0.896 injury HR: 1.4
(1.02–1.88)
0.037 failure HR: 2.7
(2.03–3.55)
<0.001 Uchino
et al [26]
LR risk OR: 2.536
(2.152–2.988)
<0.0001 injury OR: 5.412
(4.547–6.442)
<0.0001 failure OR: 10.124
(8.318–12.32)
<0.0001 Lopes
et al [29]
LR risk OR: 5.6
(1.2–26.8)
<0.001 injury OR: 6.2
(1.1–47.8)
0.008
AKI, acute kidney injury; CPH, Cox proportional hazard analysis; HR, hazard ratio; LR, logistic regression analysis; OR, odds ratio.
Trang 6on urine output criteria This may be an explanation for
the different impact of increasing RIFLE class on
mortality in the two large studies by Hoste et al
(crea-tinine and urine output criteria) [25] and Uchino et al
(creatinine criteria only) [26] Baseline mortality in
non-AKI patients was comparable Mortality in the Risk,
Injury and Failure group was, however, much higher in
the cohort studied by Uchino et al (see Fig 3), despite
the fact that the latter was a hospital wide population
and the former a general ICU population
Another limitation is the need for a baseline creatinine
level in order to calculate the proportional decrease of
kidney function A proportional increase in serum
creati-nine better represents changes in kidney function
com-pared with a severity gradation on certain cut-offs as in the
Sepsis-related Organ Failure Assessment score [9] A
patient who has an increase of serum creatinine from 0.5
to 1.1 mg/dl has a 120% decrease of kidney function and
would classify as RIFLE Injury; however, this same
patient has a renal Sepsis-related Organ Failure
Assess-ment score of 0 Baseline serum creatinine levels are
however not always known in patients who are admitted
to the emergency department or ICU If there are data,
what is the correct baseline? A serum creatinine level after
a 1.5-week hospitalization period of an elderly patient with
a pneumonia will most probably be falsely low due to loss
of muscle mass [40] Creatinine at admission is probably
less biased by loss of muscle mass; however, it may be
already elevated due to early kidney dysfunction In
patients without a history of chronic kidney disease a
standard baseline creatinine level on the basis of the
MDRD equation can be used Apart from the fact that
this can only provide an approximate value, there may also
be a question of validity of this equation The MDRD
equation was validated in a large dataset of US patients
with moderate chronic kidney insufficiency Recent
reports [41–44] from different parts of the world, however,
confirm validity in other groups of patients and ethnicities
Another issue was raised by Herget-Rosenthal et al [19]
These authors demonstrated that serum cystatin C levels
allow for earlier determination of AKI than serum
crea-tinine Although serum creatinine has its limitations, it
has been the biomarker of choice for evaluation of kidney
function for many years Recently, other biomarkers such
as cystatin C, neutrophil gelatinase-associated lipocalin,
kidney injury molecule-1 and urinary interleukin-18 have
shown promising results as an alternative [19,45–47]
Except for cystatin C, these biomarkers cannot yet be
measured in a routine setting Finally, patients classified
as Failure by RIFLE probably are a very heterogeneous
group of patients with severe AKI, with varying
pro-portions of patients treated with RRT in the different
studies Patients requiring RRT appear to have
consider-ably higher hospital mortality compared with patients
with Failure criteria who do not require RRT [25,36] Thus, a further grade designation in AKI staging may
be warranted
Future directions
Although data on AKI defined by the RIFLE criteria are increasingly reported, papers are still relatively scarce and predominantly single-centered An important step towards broader use and acceptance of the RIFLE criteria would be for a large prospective multicenter study We, and others, are currently engaged in planning for such a study
In addition, it may very well be that the spectrum of AKI may be broadened on both boundaries Maybe even more sensitive criteria for AKI and more specific criteria, e.g a 25% increase of serum creatinine or need for RRT, define meaningful subgroups of AKI patients
As patients are getting older with more comorbidity, it may also be important to put more emphasis on the acute or chronic population and expand the definition
to define subgroups with different severity grading Also, more research into the different outcome classes is needed, as literature now is very scarce
Conclusion
Small changes in kidney function in hospitalized patients are important and impact on outcome; hence, the shift of terminology from ARF to AKI RIFLE criteria provide a uniform definition of AKI and are increasingly used in the literature RIFLE severity grades represent patient groups with increasing severity of illness as illustrated
by an increasing proportion of patients treated with RRT and increasing mortality
References and recommended reading Papers of particular interest, published within the annual period of review, have been highlighted as:
of special interest
of outstanding interest Additional references related to this topic can also be found in the Current World Literature section in this issue (p 634).
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2 Eknoyan G Emergence of the concept of acute renal failure Am J Nephrol 2002; 22:225–230.
3 Davies F, Weldon R A contribution to the study of ‘war nephritis’ Lancet 1917; ii:118–120.
4 Bywaters EG, Beall D Crush injuries with impairment of renal function BMJ 1941; 1:427–432.
5 Smith HW The kidney – structure and function in health and disease Oxford: Oxford University Press; 1951.
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22
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24
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26
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28
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